FEMALE MATE CHOICE IN NONHUMAN MAMMALS

In: Animal Behavior: New Research ISBN 978-1-60456-782-3 Editors: E. A. Weber and L. H. Krause, pp 35-56 © 2008 Nova Science Publishers, Inc.

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Chapter 2

FEMALE MATE CHOICE IN NONHUMAN MAMMALS

Benjamin D. Charlton Department of Psychology, School of Life Sciences,

University of Sussex, BN1 9QH

ABSTRACT

Until now definite studies of mate choice have typically focused on non-mammal animal species where short life spans and gestation periods make reproductive success quicker to determine, and in which the females show preferences for clearly defined morphological or behavioural male traits. Mammals, which are invariably larger, have longer life spans and inter-birth intervals and are behaviourally more complex, are less suited to this type of experimentation. However, notwithstanding these difficulties, many studies of mate choice have been conducted on mammals and the current literature reveals that the females of several mammal species do appear to choose their mates, and through this potentially gain important direct and indirect fitness benefits. Here I review this body of work to reveal that the majority of female mammal mate choice studies conducted so far, particularly on large mammals, fail to: 1) determine the actual male phenotypic trait(s) of female preference (which is crucial to identifying male characteristics under sexual selection); 2) take into account other environmental and social factors that may affect female responses to male sexual signals, as well as intrinsic factors such as female hormonal state and breeding status; and 3) quantify the fitness benefits to discriminating females. I go on to give suggestions for future research and emphasise the need for a combination of carefully designed experimental and field studies. Experimental setups allow us to isolate specific male traits from other aspects of the male phenotype, determine female hormonal state and control for other competing male and female mating strategies that may affect female behaviour. Field observations of female mating behaviour can then be conducted to determine whether behavioural responses reported using experimental setups translate to actual copulations in natural conditions, and hence affect the reproductive success of individuals. Only this integrative approach will allow us to gain an appreciation of how inter-sexual selection is generated

Benjamin D. Charlton 36

on specific aspects of the male phenotype, and ultimately enable us to understand the link between mating preferences, female mate choice and reproductive success in mammals.

INTRODUCTION Sexual selection theory predicts that female mammals should preferentially mate with

high quality males, choosing the sire of their offspring for direct benefits, that increase female survival or fecundity, or indirect (genetic) benefits that increase offspring viability and/or attractiveness (Andersson 1994). Traditionally, the role of female mate choice, especially in polygynous mammals, has been considered negligible compared with male-male competition. However, on the basis of the relatively higher level of maternal to paternal investment and generally lower potential rates of reproduction the females of most mammal species could be expected to select their mating partners (Trivers 1972; Clutton-Brock and Vincent 1991). Although the fitness payoffs for discriminating females (and hence the evolutionary trajectories through which female preferences arise) are still much debated (Kirkpatrick and Ryan 1991; Jennions and Petrie 1997; reviewed by Cordero and Eberhard 2003; Kokko et al. 2003), the adaptive value of female mate choice in mammal species, where males differ in their reproductive value to females, is now generally accepted (Andersson 1994; Paul 2002).

Studies of female choice in mammals are mostly hindered by the confounding influence of other male and female mating strategies. Female mating strategies may fulfill non-procreative roles, for example, multi male mating may reflect the need to confuse paternity in mammals where infanticide is common (Wolff and Macdonald 2004) or to maintain the resources and support of male social group members (Gagneux et al. 1999). In addition, male strategies may limit a female to mating with only one male whatever her preference criteria (Soltis 1999), making it imperative to make the distinction between female mate choice and female mating preferences (Halliday 1983). Interpreting patterns of mate choice in terms of variation in mating preferences is problematic as female mating preferences, referring only to internal motivation, are just one component of female mate choice. Moreover, variation in female mate choice can be due to variability in sampling tactics, which are in turn affected by external factors (risk of predation, male harassment), as well as preference functions (Jennions and Petrie 1997). Hence, in natural conditions mating preferences are expressed in a field of environmental and social constraints imposed on mate searching females. For these reasons, female mate choice is best described “as the differential mating by females as a result of the interaction of environmental conditions, mating preferences and sampling strategies” (Wagner 1998). However, it must also be noted that females may even be passively attracted to a more conspicuous signal and not, after sampling several potential mates, actively choosing an individual at all (Forrest and Raspet 1994). Finally, mate choice is not just restricted to active discrimination between potential mating partners but can also be indirect via any other behaviour that increases or decreases the chances of mating with a specific subset of males (Wiley and Poston 1996). Any female mating strategies that incite male-male competition, e.g. reproductive synchrony (Chism and Rogers 1997) or female promiscuity (Preston et al. 2003), so that only the highest quality males can gain access to females, may represent examples of indirect mate choice.

Female Mate Choice in Nonhuman Mammals 37

Female mate choice, whether direct or indirect, is constrained by the environment and can only be realistically observed under natural conditions. However, in natural conditions male-male competition can generate the same assortative mating patterns as would female choice and it becomes hard to separate the two processes of selection (Andersson 1994). To determine female mating preferences appropriate experimental setups are required that control for male-male competition and isolate the male trait of preference from other aspects of the male phenotype. A further complication of mate choice studies lies in showing that male traits of female preference are positively correlated to male reproductive success in natural conditions i.e. that they influence reproductive outcomes, such as the viability and/or attractiveness of the offspring (Searcy and Andersson 1986). To do this requires genetic paternity analysis studies that determine the reproductive success of different male phenotypes and their subsequent offspring.

Hence, to gain a complete understanding of female mate choice in any given species requires a combination of field and experimental studies. Notwithstanding these problems, many studies of mate choice have been conducted on mammals and important insights gained. The current literature reveals that the females of several mammal species do choose their mating partners and through this potentially gain important direct and indirect fitness benefits.

FEMALE MATE CHOICE STUDIES

Choice for Direct Benefits Evidence that female mammals choose males for resources that directly increase their

fecundity or reduce reproductive costs is less abundant than it is in birds (Lampe and Espmark 2003) and insects (Thornhill 1976) but does exist. Female mate choice in some highly social mammals for more familiar males may be based on complex delayed preferences for individuals that have proved themselves better able to provision their females over time, as has been suggested in spotted hyenas (Crocuta crocuta) (East and Hofer 1991). However, conjecture aside, few studies actually show that female mammals choose mates for direct benefits or indicate what criteria are selected.

There is some evidence to suggest female choice based on territory quality occurs in certain mammal species. A study on a facultatively monogamous population of Pikas (Ochotona princeps) reports female choice of mate based primarily on nest quality and location (Brandt 1989). Females preferred single entrance dens located close to food resources for their nests, factors also positively correlated to reproductive success. In this case, males did not actively interfere with the mating attempts of other individuals and hence females may have been able to exercise relatively free choice. However, the importance of other male phenotypic characteristics not considered in this study, such as vocal displays (that could be used by females to discriminate between males) is unknown. It has also been suggested that the females of some monogamous primates may prefer males that are better able to defend a territory (Smuts 1987). However, it can be difficult in any territorial species to determine whether females are attracted to individual males per se or the territory they currently occupy. As only the highest quality males are able to acquire and hold on to the


‘preferred’ territories, any findings are probably confounded by choice for male phenotype. A further complication in quantifying female choice for territory is that it may simply be the result of females copying the preferences of other individuals (Brooks 1998) or appearing to due to the incidental consequence of some other adaptive behaviour e.g. females congregating together to reduce predation risk or harassment (Clutton-Brock and McComb 1993).

Iberian red deer males (Cervus elaphus hispanicus) compete for and defend territories that females are subsequently attracted too (Carranza 1995). Although male phenotype would still appear to be important for attracting females, as some males maintained higher attraction rates than others on the same territories, male reproductive success in this species seems to be largely dependant on the quality and/or position of territory held. Some other studies on polygynous ungulates have suggested female mate choice based at least partly on territory at leks (Apollonio et al. 1990; Balmford et al. 1992a). These mating systems are traditionally thought to provide only indirect benefits to females, however, female choice driven at least in part for direct benefits would go some way to solving what has become known as the 'lek paradox' (Borgia 1979; Reynolds and Gross 1990).

Other studies have suggested that female mammals obtain direct benefits in the form of reduced harassment when selecting to mate with males on leks (Balmford 1991; Clutton-Brock et al. 1992; Nefdt and Thirgood 1997). However, this is also disputed by work reporting higher rates of harassment for females on leks (Bro-Jorgensen 2002). In any case, harassment by other courting males can impose serious fitness costs which mate searching females would be expected to avoid (Reale et al. 1996). It would appear that certain female mating tactics have evolved to reduce male harassment costs (Galimberti et al. 2000) and females may also be expected to have evolved preferences for males with certain characteristics that can reduce disturbances from other males. This appears to be the case in South American sea lions (Otaria flavescens: Cassini and Fernandez-Juricic 2003) and possibly Sumatran orangutans (Pongo pygmaeus abelii: Fox 2002) where female association with adult males, to reduce harassment costs, may be a factor influencing mate choice. Female attraction to males with higher roaring rates in red deer (Cervus elaphus) may also reflect a choice for high quality males that are better able to protect females from harassment and hence a choice based partly on direct benefits to the female (McComb 1991).

In mammals where parental care limits female reproductive success females could be expected to show a choice for males that demonstrate infant care abilities. Some male primates occasionally carry infants and, as carrying may reduce the risks of infanticide and hence be of direct benefit to the female, this could be seen as a form of parental care (Palombit et al. 1997). However, this care may simply be a male mating strategy if females mate preferentially with males that have previously demonstrated infant care (Keddy-Hector 1992). In male lions (Panthera leo) mane darkness is correlated to serum testosterone and nutrition, reflecting good fighting ability and short-term health of the bearer (West and Packer 2002). Thus, females could gain direct benefits from preferring males with darker manes that would be more adept at protecting their cubs from infanticide and providing food for the pride. These predictions remain untested and currently there appears to be no documented cases of female choice based on parental care abilities in mammals. However, some monogamous mammals could be expected to exhibit bi-parental care, as certainty of paternity for males would be higher than it is in polygynous mammals. More research is required to determine whether or not this is the case. Lastly, there may also be direct incentives for females to avoid parasitized males in mating systems where the female appears to gain


nothing more from than a male’s sperm from copulation (Kirkpatrick and Ryan 1991). Effects of parasite infection on mate choice may therefore reflect the avoidance of direct costs, if fecundity is affected by parasite infection, rather than Hamilton-Zuk style indicator systems.

Choice for Indirect (Genetic) Benefits In mating systems where males contribute little but their genes to their offspring it may

be that females are choosing males for the indirect benefits of ‘good genes’ (Darwin 1871; Maynard Smith 1991). The expression of a specific morphological trait of preference in the offspring whether it advertises ‘genetic quality’ or is arbitrarily ‘attractive’ to females will yield higher lifetime reproductive success via increased longevity or mating opportunities for the bearer (Kokko et al. 2002). Female mate choice for male phenotype is undoubtedly important in lekking mammals (Clutton-Brock et al. 1989; Balmford 1991; Bro-Jorgensen 2002) but the exact criteria on which female preferences are based in these mating systems is still fairly unclear. The majority of mate choice studies conducted so far on mammals claim to demonstrate female preferences for dominant individuals. As high status may indicate high genetic quality, this suggests that choice for ‘good genes’ may be an important selective force in mammals.

A recent study investigating the relationship between male dominance ranks, female mate choice and reproductive success in captive chimpanzees (Pan troglodytes) reports female choice for dominant males (Klinkova et al. 2005). However, in this case, the positive correlation between male dominance rank and reproductive success observed would appear to be generated predominantly by rank related differences in female solicitations and competitive ability. Indeed, with a social climate characterized by male coercion, in which females are unlikely to be able to exercise free choice, it may be impossible to determine whether any choice reflects true underlying female preferences. Dominant males will often monopolize access to females during the breeding season or at peak conception time (Soltis 1999; Preston et al. 2003), especially in mating systems where female mating tactics incite male-male competition (Semple 1998; Wolff 1998). Other researchers investigating mammal mate choice in natural conditions, propose that females choose dominant or more vigorous males on the basis that subordinates are rejected: reindeer (Rangifer tarandus: Hirotani 1989); bighorn sheep (Ovis canadensis canadensis: Hogg 1987); pronghorn deer (Antilocapra americana: Byers et al. 1994) and bison (Bison bison: Wolff 1998) or because female solicitation rates are higher to dominant individuals: chimpanzees (Pan troglodytes: Matsumoto-Oda 1999; Vorobieva et al. 2004); Japanese macaques (Macaca fuscata: Soltis et al. 1997); ring-tailed mouse lemurs (Lemur catta: Parga 2002) and vervet monkeys (Cercopithecus aethiops: Keddy 1986). However, the findings of the above studies cannot be interpreted as evidence for active female choice of dominant males when in actual fact the female’s ability to express preferences is likely to be constrained by the social environment. In addition, avoidance of young or subordinate males by females is common in several mammal species (Cox and Leboeuf 1977; Clutton-Brock et al. 1982; Miura 1984; Hirotani 1989; Komers et al. 1999) and hence, whether females are directly choosing dominant individuals remains speculative.

When other competing males are around there are likely be other reasons for associating with older or more dominant individuals who may be expected to have greater abilities to


acquire and defend resources as well as provide increased protection from sexual coercion, harassment or infanticide (Pope 1990; Pereira and Weiss 1991). Indeed, female capuchins cease to prefer the dominant male when he loses his dominance status, suggesting that they are not selecting these individuals for their ‘good genes’ (Janson 1984). Moreover, dominant male mammals do not always consistently attain high reproductive or even mating success (Takahata et al. 1999). In any case, it is imperative to control for male competition so that female mate choice can be studied free of constraints and mating preferences can be determined.

Experimental Studies of Female Preferences in Mammals

Until now definite experimental studies of mate choice have typically focused on non-mammal animal species e.g. insects (Klappert and Reinhold 2003), frogs (Murphy and Gerhardt 2000) and birds (Mountjoy and Lemon 1996) where short life spans and gestation periods make reproductive success quicker to determine and in which the females show preferences for clearly defined morphological or behavioural male traits. Mammals, which are invariably larger, have longer life spans and inter-birth intervals and are behaviourally more complex, are less suited to this type of experimentation. Notwithstanding these problems, some studies on small mammals reporting direct female mate choice for dominant males have controlled for male competition using laboratory experiments: house mouse (Mus musculus: Rolland et al. 2003; Tomihara 2005) and field experiments: golden hamsters (Mesocricetus auratus: Lisk et al. 1989); brown lemmings (Lemmus-Trimucronatus: Huck and Banks 1982); voles (Microtus ochrogaster and Microtus montanus: Shapiro and Dewsbury 1986); bank voles (Clethrionomys glareolus: Horne and Ylonen 1996) and brown capuchins (Cebus apella: Janson 1984; Welker et al. 1990). However in all these cases, the exact male phenotypic trait(s) of female preference are not known.

A recent experiment on captive grey mouse lemurs (Microcebus murinus) employed a two-way mate choice design in which females could choose between two separately caged males, hence controlling for male-male competition (Craul et al. 2004). The authors report a consistent spatial and/or behavioural female preference, during oestrus, for the male with the higher trill call activity. However, as the authors report, higher trill rate is also positively correlated to male dominance rank and hence, it is impossible to determine whether females are actually attracted to calls with higher trill rates or if this is simply a by-product of this correlation. In addition, only 4 copulations (out of 12 females) were observed and hence whether these preferences translate to increased mating, or more importantly, reproductive success is unknown i.e. whether mating with males with higher trill call activity actually increases offspring viability. Indeed, an earlier study on the same species of mouse lemur reports that dominant males only sired half the offspring in a captive environment in which they may be expected to be able to monopolise females (Radespiel et al. 2002). Another study on the wild guinea pig (Galea musteloides), controlling for male competition, reports female preferences for heavier and more frequently courting males (Hohoff et al. 2003). However, in this case the high degree of promiscuity shown by the females suggests that sperm competition may be of greater importance than pre-copulatory mate choice. In this species, as with several primates, mating with larger more dominant males may fulfil other non-procreative functions and again, evidence that it results in more viable offspring is lacking.

In theory, females may also be expected to mate with older males for genetic benefits because viability selection leads to older males with higher genetic quality than those that are


younger (Trivers 1972; Kokko and Lindstrom 1996). This theory is backed up to some extent by studies reporting female preferences for older males in birds and insects (Simmons and Zuk 1992; Grahn and Vonschantz 1994). Although no empirical evidence exists in mammals, older males may also be preferred where age attests to viability in the current environment. In spotted hyenas (Crocuta crocuta) it has been suggested that male tenure may serve as an index of intrinsic genetic quality, although male fertility may also decline with extreme old age (East et al. 2003). Indeed, a recent theoretical model by Beck & Powell (2000) suggests that preferences for older males are unlikely to evolve in mating systems in which the male provides only sperm. In any case, empirical evidence for increased offspring viability would be required to determine whether females are actually choosing older males for their ‘good genes’. In fact, it appears that the only demonstration of increased progeny viability due to free female mate choice in mammals has been carried out on house mice (Mus musculus) (Drickamer et al. 2000). In this study, females that were allowed to choose their mates produced offspring of greater viability than those mated at random. However, although this represents empirical evidence of female mate choice for ‘good genes’, the actual male phenotypic trait(s) of female preference are again not known.

Indeed, identifying the actual trait of female preference, which is crucial to identifying male characteristics under sexual selection, can be extremely difficult. In addition, female preferences in many mammals may only emerge at specific times such as oestrus (Poole 1989; Matsumoto-Oda 1999; Pillay 2000) or in particular contexts (Qvarnstrom 2001) and in any case, seem likely to be based on multiple cues to male quality, of different or the same modalities (Candolin 2003). It follows therefore that in order to gain a foothold in this immensely complex subject, we must use appropriate experimental setups that control adequately for all other extrinsic and intrinsic factors that affect female behaviour, and in which specific phenotypic traits are isolated from other aspects of the male phenotype. Female responses to variation in specific signal components can then be assessed and an appreciation of how inter-sexual selection is generated on specific aspects of the male phenotype can be gained.

Female Preferences for Specific Phenotypic Traits Signalling Male Genetic Quality

Preliminary evidence that females of some mammal species may choose males for specific phenotypic traits comes from experimental set ups which are able to isolate specific male traits from other aspects of the male phenotype. However, conclusively demonstrating ‘attraction’ to an isolated trait variant, and hence inferring that mate choice decisions could be made based on them, is difficult.

Among mammals, primates possess the most brilliant secondary sexual colouration that may serve to advertise the bearer’s quality to potential mates. Examples include the brightly coloured faces of male mandrills (Mandrillus sphinx) (Setchell and Dixson 2001) and scrotal colour in vervets (Cercopithecus aethiops) (Gerald 2001). Whether female mandrills or vervet monkeys attend to these colour differences between males, however, is unknown. Rhesus macaque females (Macaca mulatta) gaze for longer at computer-manipulated red over pale versions of male faces (Waitt et al. 2003). In this case, male coloration might provide a cue to male quality but to determine whether these visual preferences indicate sexual preferences rather than constituting a more general response requires further research. Female preferences for darker manes have been demonstrated in lions (Panthera leo) (West and Packer 2002). Darker manes increase heat load for the male lions and may represent an honest indicator of


‘good genes’ (handicap theory: Zahavi 1975), as males with darker manes are presumably better able to withstand heat-related costs. Indeed, the study reports that males with the darkest manes had superior survival and competitive abilities resulting in increased offspring fitness, but that mane darkness was not heritable. It appears that male colouration, by indicating genetic quality, may play a part in adaptive female mate choice in mammals. Designing appropriate mate choice experiments to answer this question remains a challenge for the future.

Olfactory cues are relatively simple to isolate and present to females in controlled conditions and some of the best evidence of mate choice for ‘good genes’ in mammals has been generated in this way. Female mice (Mus domesticus) and rats (Rattus rattus) appear able to discriminate between parasitized and non-parasitized males based on urine odours (Willis and Poulin 2000; Kavaliers et al. 2003) and display increased stress responses to the urine odours of parasite-infected males (Kavaliers et al. 1998). In addition, female house mice mate preferentially with non-parasitized individuals (Ehman and Scott 2002), possibly securing resistant, and hence, ‘good’ genes for their offspring (Hamilton and Zuk 1982). Female odour preferences for resident males are also reported in rabbits (Oryctolagus cuniculus) (Reeceengel 1988) however, if these males actually achieve higher reproductive success in natural conditions remains unknown.

Scent over-marking is a common form of competitive advertisement among many mammal species and some work has suggested that scent frequency and placement may play a role in mate choice, possibly for dominant males that mark over subordinates (Johnston et al. 1997; Johnston and Barot 2004) . The Johnston et al. (1997) study on meadow voles (Microtus pennsylvanicus) reports female preferences for familiar over novel males even when their scents have been over marked by novel males; however, the ability of these females to discriminate between either novel or familiar male scent markings placed on top of each other could be disputed. Indeed, studies on prairie voles (Microtus ochrogaster) in which mate choice based on these criteria had been hypothesised but subsequently disproved, suggests that scent quality may be more important than scent frequency and placement for mate attraction (Thomas 2002; Mech et al. 2003).

Vocal displays can also be reproduced accurately and isolated from other aspects of the male phenotype using playback experiments. Several previous studies on mammals have suggested that male calls may function directly to advertise male quality and attract females without testing experimentally whether or not this is the case: old world monkeys (Gautier and Gautier 1977); pikas (Ochotona princeps) (Conner and Whitworth 1985); hammerhead bats (Hypsignathus monstrosus) (Bradbury 1977); and some ungulates (Kiley 1972; McElligott et al. 1999). The structurally complex songs of lone humpback (Megaptera novaeangliae) and finback whales (Balaenoptera physalus) and the underwater acoustic displays of male harbour seals (Phoca vitulina) are also thought to function in broadcasting male quality and attracting females (Tyack 1981; Hanggi and Schusterman 1994; Croll et al. 2002). More detailed work on humpback whales, although confirming that these acoustic displays mediate approach and avoidance response, reports no female attraction to male song (Tyack 1983; Mobley 1988). However, the possibility that the female humpbacks use male vocal displays to assess potential mates, only allowing certain males to approach them, cannot be excluded. Similarly, although the long calls of male orangutans (Pongo pygmaeus) were originally thought to function in mate attraction, playback experiments to specifically test this


did not yield the predicted results (Mitani 1985). This further highlights how crucial it is to test predictions about mate choice using systematic playback experiments.

Recent work on fur seals (Arctocephalus spp.) suggests that the divergence in bark calls (which are only given during male-female interactions) could be due to female choice but not full threat calls directed at other males (Page et al. 2002). Indeed, although female mate choice is very likely to be a significant selection force on the calls of many male mammals, currently, the only mate choice studies conducted on any mammal that systematically demonstrate a female preference for a vocal characteristic are in red deer (Cervus elaphus) (McComb 1991; Charlton 2006; Charlton et al. 2007b). The McComb (1991) study demonstrated a female preference for male roars delivered at higher rates. As male roaring is energetically costly to produce this may represent an honest signal of genetic quality e.g. a handicap (Zahavi 1975; Grafen 1990) and hence a choice for good genes; however, roaring rate seems more likely to reflect current short-term condition or motivation rather than long-term genetic quality. More recent work using an experimental setup showed that oestrous female red deer preferred male roars in which lower formant frequencies simulated larger caller’s (Charlton et al. 2007b). To date, this remains the only female mate choice study in mammals to demonstrate a mating preference for an isolated male phenotypic trait signalling ‘good genes’ (i.e. larger body size) whilst controlling for female hormonal state and male-male competition.

Choice for Compatible Genes Another aspect of female choice for male genetic ‘quality’ concerns genetic compatibility

(Trivers 1972; Neff and Pitcher 2005) with an increasing body of empirical studies to suggest that females should benefit, by increasing offspring fitness, through choosing genetically dissimilar males (Mays and Hill 2004). Indeed, choice for unfamiliar or novel partners as suggested in several mammals may function to increase offspring genetic heterozygosity and subsequent fitness (Manson 1995; Amos et al. 2001). However, in these cases females should choose in a relative rather than an absolute sense and prefer males with genotypes that best complement their own rather than for ‘good genes’ per se. This method of mate selection does not lead to genetic fixation of male traits, a problem for good genes and runaway selection models, as females should not be congruent in their choice for particular male phenotype i.e. a male that is best for one female may not be best for another (Brown 1997). Choice for compatible genes may have evolved to avoid the reproductive costs associated with inbreeding and distant outbreeding. Female white-footed mice (Peromyscus leucopus) gain maximum reproductive success when mated with males of intermediate genetic similarity (Keane 1990) and may represent an example of this type of mate choice, but how the mating preferences observed in this study are mediated is unclear. Indeed, the major problem facing the theory of female choice based on genetic compatibility is in how females actually recognise genetically incompatible mates.

There is good evidence to suggest that the genes of the major histocompatibility complex (MHC), that play a key role in the immune system, function as cues to mate choice for genetically compatible males (reviewed in Penn and Potts 1999). Generally, the mating preference seems to be MHC-disassortative i.e. males with dissimilar major histocompatibility complex alleles are preferred (Penn 2002). This mating pattern leads to


more outbred and heterozygous offspring, which has been suggested to increase offspring fitness (Brown and Eklund 1994; Grob et al. 1998). Indirect evidence for MHC mediated inbreeding avoidance comes from Potts et al. (1991) who, having found significantly fewer MHC-homozygous offspring than expected, suggested that female mice (Mus domesticus) sought extra-territorial copulations with MHC dissimilar males. However, the results of this study may be the product of simple non-MHC mediated inbreeding avoidance. Convincing evidence for MHC-disassortative mating preferences in mammals has been generated by work on captive mice (Mus domesticus) where discrimination between different MHC genotypes seems to be mediated through specific odour cues (reviewed by Jordan and Bruford 1998). MHC-disassortative mating preferences may increase the resistance of offspring to infectious diseases (Penn 2002) and/or enable individuals to recognize closely related kin and function to avoid inbreeding (Yamazaki et al. 2000). Since MHC genes influence resistance to many infectious diseases, females who prefer disease resistant males may confer these resistant alleles on their offspring (Hamilton and Zuk 1982), however, it remains to be shown whether males with attractive displays carry resistant MHC alleles. Indeed, it is not clear whether the main function of MHC-disassortative mating preferences is enhanced progeny immunocompetance or inbreeding avoidance. Either way, there are potential indirect fitness benefits available to discriminating females.

MHC-dependant preferences may exist across several mammal species. For example, MHC variation is related to antler development and body mass in white tailed deer (Odocoileus virginianus) and hence indicates ‘good genes’ (Ditchkoff et al. 2001). Interestingly, although MHC variation in soay sheep (Ovis aries L.) is associated with resistance to a parasitic nematode (Paterson et al. 1998) no evidence for MHC-disassortative mating preferences exists in this species (Paterson and Pemberton 1997). In this case, any female preference may have been masked by intense male-male competition but nevertheless demonstrates the need to test these predictions. Theoretically, female preferences for common MHC alleles, and hence genetic similarity at these loci, could also arise where an evolutionary ‘arms race’ type scenario exists between hosts and parasites that have not yet adapted to recently common alleles (Hamilton and Zuk 1982). Female striped mice (Rhabdomys pumilio) prefer ‘homotype’ males from their own population than ‘heterotype’ males, a preference for genetically similar males possibly mediated by MHC alleles (Pillay 2000). However, inbreeding avoidance would appear to offer the highest potential fitness benefits to females (Penn 2002). A recent study on wild house mice (Mus domesticus) reported that inbred males sired only one fifth as many surviving offspring as outbred males (Meagher et al. 2000). Female choice for unfamiliar or novel partners is observed in several mammals (Manson 1995) and may in some cases be mediated by MHC gene complexes in mammal species at risk of inbreeding (Clarke and Faulkes 1999; Valsecchi et al. 2002). While there is much evidence that MHC-dependant mating preferences exist in house mice further research is required to determine their generality to other mammal species.

Post-copulatory Choice Post-copulatory or ‘cryptic’ mate choice, in which females selectively abort the sperm or

offspring of certain males, can take two forms; directional post-copulatory choice in which females bias sperm use after copulation towards certain male phenotypes and non-directional


in which females favour the sperm of males with compatible genotypes regardless of their phenotype.

The copulation calls of some female primates that, by encouraging mate guarding and minimizing sperm competition, increase the chances of fertilization by preferred males may represent an example of directional post-copulatory mate choice in mammals (Maestripieri and Roney 2005). This is a compelling argument and contrary to previous suggestions that these copulation calls function to increase sperm competition (Oconnell and Cowlishaw 1994; Semple 1998). Indeed, an earlier study on barbary macaques (Macaca sylvanus) also reported increased mate guarding by consort males in response to copulation calls, which again is consistent with the post copulatory choice hypothesis (Todt et al. 1995).

Non-directional post-copulatory mate choice can take place via mechanisms that have evolved to prevent females from being fertilized by incompatible sperm (Zeh and Zeh 1996; Zeh and Zeh 1997). There is evidence in mice (Mus domesticus) that MHC-derived proteins expressed on sperm may influence the likelihood that a given spermatozoan will fertilise the egg, with MHC-similar pregnancies spontaneously aborted (Rulicke et al. 1998). Conversely, female grey mouse lemurs (Microcebus murinus) actively delay pregnancies more when housed with unfamiliar males suggesting post-copulatory choice for familiar males (Radespiel and Zimmermann 2003). Whatever the preference, post-copulatory mate choice may represent a powerful selective force, especially in mating systems dominated by male coercion and in which females are unlikely to be able to exercise pre-copulatory mate choice.

CONCLUSION Female mate choice in mammals represents a challenging area of research with many

questions still to be answered. While it appears that female mammals are provided with important direct and indirect benefits through mate choice, the functions and evolutionary consequences of such choice remain unclear. To answer these questions, definite evidence of how mate choice for particular male phenotypes impacts on female fecundity and reproductive success is required. If direct benefits are available, they are likely to have a much greater effect on female fitness than indirect benefits, and selection for males providing such benefits is easy to understand (Price et al. 1993). Surprisingly, although direct benefits may provide a possible explanation for some female mammal mating tactics (Wolff and Macdonald 2004), empirical evidence for mating preferences based on them is distinctly lacking in mammals, although direct fecundity benefits may underlie some mating preferences on leks. This apparent omission may arise because the majority of mate choice studies so far have been conducted on polygynous mammals in which males appear to provide little, if any, direct benefits to females and subsequently where female preferences based on them would be harder to observe. Mate choice for indirect benefits, because it is generally assumed that it will result from a genetic association between male attractiveness and offspring fitness, has always been controversial and considered insufficient to explain the evolution of female mating preferences alone (Kirkpatrick 1996). However, a recent theoretical model by Moller & Jennions (2001) suggests that direct benefits are only slightly more important than indirect ones arising from female choice. In reality, female mate choice in most mammal species will almost certainly be influenced to some extent by both direct and


indirect benefits. A study on puku (Kobus vardoni) and topi antelopes (Damaliscus lunatus) in which male phenotype, predation risk and territory quality were all related to female presence appears to confirm this (Balmford et al. 1992b). However, because putative mate choice cues are often interrelated, their relative importance for mate choice becomes difficult to ascertain.

A major problem with the majority of mammal studies is in how female preferences are quantified. Many experimental studies rely on indirect methods to assay female preferences such as increased attention towards an isolated male trait, which does not necessarily indicate attraction. For example, greater attention by red deer hinds to roars simulating males of sub-adult body size than to those simulating a large adult male, whilst making no sense from a mate choice perspective, is likely to indicate an aversive response to facilitate earlier detection and avoidance of young stags that are known to harass them (Charlton 2006; Charlton et al. 2008b). Observational studies often use high levels of interaction with certain individuals, which may be due to social and/or environmental constraints or for non-procreative reasons, to suggest a mating preference. In addition, many of these studies only record mating success, as individuals gaining copulations or proximity to members of the opposite sex, and do not necessarily record the reproductive success of individuals. It is essential to conduct genetic paternity analysis studies, to determine the reproductive success of trait bearing individuals and their offspring in natural environments, and hence determine any reproductive benefits to choice. Moreover, realistic assessments of the costs of female mate choice need to be carried out under approximately natural conditions when food supplies are limited and predators and competitors are present. These limitations on obtaining accurate measures of the costs and benefits of mate choice, as well as interacting and often competing male and female mating strategies, make it difficult to test theoretical predictions on mammals.

Some theoretical models of female mate choice behaviour suggest that females should be flexible in their mate choice decisions (Real 1990; for a review see Jennions and Petrie 1997) and recent empirical data shows plasticity of female preferences in animals (Moore and Moore 2001; Veen et al. 2001; Welch 2003; Chaine and Lyon 2008) even during a single reproductive cycle (Lynch et al. 2005). Studies of female choice in mammals, in which female preferences may only emerge during the period of peak conception, also emphasize the importance of considering the timing of female ovulation (Matsumoto-Oda 1999; Stumpf and Boesch 2005). Recent work on oestrous female red deer demonstrated a mating preference for male roars simulating larger caller’s (Charlton et al. 2007b), a trait positively correlated to male reproductive success in this species (Reby and McComb 2003). Importantly, by using an experimental setup, this study not only controlled for female hormonal state but was also able to remove other environmental and social factors that may otherwise obscure female mating preferences. Indeed, studies on other animals without observable female mate choice in natural conditions have illustrated that otherwise hidden female preferences do in fact exist and emerge under appropriate experimental conditions (Gould et al. 1999).

Future work should follow this type of experimental approach and concentrate on demonstrating female preferences for specific male traits using setups that control for the effects of male and female mating strategies and female hormonal state. Experimental investigation of female preferences, because they are highly dependant on female hormonal state, should be conducted during and outside peak conception times. Comparisons of female


reproductive behaviour during and outside peak conception times has yielded interesting results in tungara frogs (Physalaemus pustulosus) (Lynch et al. 2005) and house mice (Mus musculus) (Rolland et al. 2003) and may similarly provide important insights into female mate choice in large mammals. Female preferences are also likely to vary geographically due to evolved genetic/environmental differences (Qvarnstrom 2001). Therefore, interesting comparisons could also be made of the female mating preferences of a given mammal species in different environmental conditions. Moreover, experiments using repeated measures designs would provide more complete information about the form of female preferences in mammals, enabling preference functions (how the strength of a female preference varies according to the expression of the male trait) to be built up for individual females as well as for populations (Wagner 1998). In addition, as mate choice studies in general have paid less attention to variation between individual females than males (Jennions and Petrie 1997) the examination of both within and between-female variation in preferences may prove to be a productive area of research in mammals.

Mate-searching females are also likely to assess multiple cues when making mate choice decisions (Candolin 2003; van Doorn and Weissing 2004), yet no mammal mate choice studies have explicitly examined the relative importance of different male traits to female choice. To do this would require experiments in which different male phenotypic trait values within a stimulus are independently varied and presented to females in order to ascertain their relative importance for mate choice. In particular, this approach would allow us to examine how male traits interact to influence female mating decisions. Such interactions undoubtedly have important implications for sexual display evolution in animals’ generally e.g. satin bowerbirds (Ptilonorhynchus violaceus: Patricelli et al. 2003) and appear to have important effects on female mate choice behaviour in some anuran (Hyla gratiosa: Poole and Murphy 2007) and insect species (Gryllus campestris: Scheuber et al. 2004), but as yet represent an unexplored avenue of research in mammals. A recent study on red deer independently manipulated components of the male roar, the fundamental frequency and the formant frequencies (an acoustic cue to body size), in order to examine female looking responses to calls characterized by different combinations of these acoustic components (Charlton et al. 2008a). The findings of this study suggested that the fundamental frequency of the male roar did not affect female perception of size-related formant information but also reinforced the idea that formants, being a long-term indicator of male body-size and hence genetic quality, are more important to red deer hinds as acoustic cues for mate assessment during the breeding season. Future mammal studies should follow this approach to examine the combined effect of variation in two separate components of a male mammals sexual display, using experimental setups in which the effects of competing male and female mating strategies, female hormonal state and female sampling strategies are controlled for.

In conclusion, female mate choice in mammals remains a complex research area requiring new and innovative experimental paradigms to elucidate what are often transient female preferences. Technological advances in digital sound production and playback equipment make female preferences for vocal characteristics, which can easily be isolated, a possible area for advancing our knowledge of female mate choice. Playback experiments can be used to present females with re-synthesized male calls, in which a vocal characteristic of interest is manipulated, to test their ability to perceive cues to male quality in mammal calls (Charlton et al. 2007a), and investigate whether they use these cues to assess male quality in a mate choice context (Charlton et al. 2007b.). Other technological advances now allow digital


images to be realistically modified to test for visual preferences (Waitt et al. 2003) or to test the ability of females to link acoustic stimuli to visual representations of different male phenotypes (Ghazanfar et al. 2007). This experimental work should be followed up by fieldwork where mating behaviour can be observed and paternity analyses conducted under natural conditions to realistically determine the reproductive outcomes of male and female mating strategies. By combining knowledge gained from experimental and observational studies both in the field and laboratory we may ultimately hope to understand the link between mating preferences, female mate choice and reproductive success in mammals. Only a combination of carefully designed field and laboratory experiments will enable us to achieve this goal.

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FEMALE MATE CHOICE IN NONHUMAN MAMMALS

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